Transcriptome Sequencing of Epipogium (Orchidaceae) and Monotropa (Ericaceae) Reveals Parallel Gene Losses in Nuclear Genomes of Non-Photosynthetic Plants

Holoheterotrophy, i.e. a total inability to photosynthesize, has arisen independently multiple times in different plant lineages. While changes in plastid genomes of holoheterotrophic plants are widely studied, little is known about changes in nuclear genomes accompanying transition of plants to completely heterotrophic lifestyle. In order to gain insight into this question we sequenced and assembled transcriptomes of non-photosynthetic plants from two phylogenetically distant groups: monocots (Epipogium aphyllum and E. roseum) and dicots (Monotropa hypopitys). Earlier we characterized plastid genomes of these plants and found that they are highly reduced: only components of translation system and several other housekeeping genes remain intact. Comparative analysis with transcriptomes of related photosynthetic species was used to highlight changes inherent to nuclear genomes of these plants.

Almost all changes that we found are associated with the loss of photosynthesis, e.g., the loss of nuclear genes encoding components of plastid electron-transfer chain, proteins of light-harvesting complex, components of RuBisCo etc. Surprisingly, we found that genes encoding chlorophyll a synthesis pathway proteins are intact in Epipogium and, presumably, in M. hypopitys. The same feature was previously reported for broomrape Phelipanche aegyptiaca. Also, there are several reports stating that chlorophyll a is present in many holoheterotrophic plants, including Monotropa uniflora, a close relative of M. hypopitys. The reasons for such conservation are yet unclear; we believe that further study of transcriptomes of non-photosynthetic plants will shed light on this question, as well as on other aspects of nuclear genome/plastome coevolution under loss of photosynthetic activity.